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Article (refereed) - postprint
May, Linda; Spears, Bryan M.; Dudley, Bernard J.; Gunn, Iain D.M. 2014. The
response of the rotifer community in Loch Leven, UK, to changes
associated with a 60% reduction in phosphorus inputs from the
catchment [in special issue: Rotifera XIII] International Review of
Hydrobiology, 99 (1-2). 65-71. 10.1002/iroh.201301705
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May et al – Rotifers in Loch Leven
1
LINDA MAY1 (CORRESPONDING AUTHOR), BRYAN M. SPEARS1, BERNARD J. DUDLEY1
2
AND IAIN
D.M. GUNN1
3
4
1
NERC - Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian EH26
5
0QB, UK.
6
7
Research Paper
8
The response of the rotifer community in Loch Leven, UK, to
9
changes associated with a 60% reduction in phosphorus inputs
10
from the catchment
11
12
13
Corresponding author contact details:
14
Dr. L. May,
15
NERC - Centre for Ecology & Hydrology,
16
Bush Estate,
17
Penicuik,
18
Midlothian EH26 0QB
19
UK
20
Email: lmay@ceh.ac.uk;
21
Phone: +44(0) 131 445 4343
22
23
key words: lake, eutrophication, phosphorus, rotifers, recovery, restoration, indicator,
24
zooplankton
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May et al – Rotifers in Loch Leven
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Abstract
26
Lakes across the world are suffering from anthropogenically induced nutrient
27
enrichment problems and many attempts are being made to improve their water
28
quality and ecosystem function. Most metrics that are being used to monitor recovery
29
are based on relationships that have been established across a range of lakes. These
30
may not respond quickly to in-lake changes in water quality when nutrient
31
management strategies are put in place. This paper uses data routinely collected from
32
Loch Leven, UK, to examine the immediate and longer-term responses of the rotifer
33
community to a 60% reduction in phosphorus input from the catchment in the early
34
1990s. We conclude that changes in rotifer abundance and relative species
35
composition are sensitive indicators of lake-specific changes in water quality,
36
responding more quickly than more widely used metrics, such as total phosphorus and
37
chlorophyll a concentrations. However, like all indicators of change, such indices
38
must be used with care in situations where rotifer populations are subject to multiple
39
stressors.
40
41
1. Introduction
42
43
Lakes across the world are suffering from anthropogenically induced nutrient
44
enrichment problems and many attempts have been made to improve their water
45
quality and ecosystem function by reducing inputs from the catchment. However,
46
only in a small number of case studies have the results of such interventions been
47
recorded for long periods of time after nutrient management strategies have been put
48
in place (e.g. see examples reviewed by Jeppesen et al. 2005). Even fewer studies
2
May et al – Rotifers in Loch Leven
49
have reported the impacts of management intervention on the rotifer community of
50
specific lakes.
51
52
Rotifers have long been recognised as good indicators of water quality across a range
53
of lakes (e.g. Maemets 1983; Pejler 1981; Pejler 1983; Sladeček 1983; Matveeva
54
1991; Duggan et al. 2001; Ejsmont-Karabin 2012), but it is unclear whether they can
55
be used as indicators of temporal change within a single site in response to restoration
56
measures. This is because most of the relationships between rotifer species
57
composition and abundance, and lake trophic state, have been based on contemporary
58
comparisons of rotifer communities across multiple lakes (e.g. Berzins & Pejler 1989;
59
Jeppesen et al. 2000; Duggan et al. 2001; Tasevska et al. 2012) rather than in-lake
60
changes over time. In general, although the rotifer community is an important
61
component of lake food webs, the way that it responds to change is poorly
62
understood. This is because our knowledge is limited to the results of relatively few
63
long-term studies (e.g. Matveeva 1986; Walz et al. 1987; Balvay & Laurent 1990;
64
Ejsmont-Karabin 1996), some of which have not linked the responses of the rotifer
65
communities that they describe to changes in environmental pressures over time (e.g.
66
Muirhead et al. 2006; Steinberg 2009).
67
68
Rotifer communities have been shown to respond quickly to a wide range of
69
environmental stresses such as acidification, climate change, eutrophication and metal
70
pollution (Walz et al. 1987; May & O’Hare 2005; Havas et al. 1995; Svensson &
71
Stenson 2002; Vbra et al. 2003; Waeervagen & Nilssen 2003; Dupius & Hann 2009).
72
Of these, the impacts of changing eutrophication pressures have received the most
73
attention (Matveeva 1986; Walz et al. 1987; Ejsmont-Karabin & Hillbricht-Ilkowska
3
May et al – Rotifers in Loch Leven
74
1994). Once these pressures have been reduced, as with other freshwater biota,
75
‘recovery’ may not necessarily be characterised by the reversal of the patterns that
76
were observed during degradation. For example, recent studies have suggested that
77
zooplankton community responses in lakes can be delayed for many years, and by a
78
number of confounding factors, when phosphorus (P) inputs from the catchment are
79
reduced. These include changes to other chemical stressors (e.g. acidification), fish
80
stocking practices, climate change, persistent internal P loading and (e.g. Jeppesen et
81
al. 2005).
82
83
With a few notable exceptions (e.g. Lake Peipsi – Haberman et al. 2010), most long
84
term studies of rotifers have focused on the impact of eutrophication, but not of re-
85
oligotrophication, on the planktonic community. So, reports on the recovery of the
86
rotifer community, once nutrient inputs have been reduced, are relatively rare. This
87
paper documents the responses of the rotifer community in Loch Leven, UK, over a
88
34 year period that is characterised by three key periods of eutrophication and nutrient
89
management: (1) pre-management (1977-1982); (2) nutrient reduction and immediate
90
post-management (1991-1998); and (3) longer-term post-management (2010-2011).
91
Routine monitoring at this site since 1968 has provided a long time series of physical,
92
chemical and biological variables with which to explore the response of the rotifer
93
community to the nutrient reduction process.
94
2. Methods
95
96
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Study site
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Loch Leven (56o 10’ N, 3o 30’ W) is a large (13.3 km2), shallow lake in the east-
99
central Scotland, UK, with mean and maximum depths of 3.9 m and 25.5 m,
100
respectively (Kirby 1971). The lake has an average hydraulic retention time of about
101
5.2 months (Smith 1974) and drains a predominantly agricultural catchment of about
102
145 km2. Several small towns and villages within the catchment have a total
103
population of about 11,000 people (Frost 1996).
104
105
Loch Leven is, primarily, phosphorus (P) limited and has a long and well documented
106
history of eutrophication and recovery (May & Spears 2012). Between 1985 and
107
1995, total phosphorus (TP) inputs from the catchment were reduced by about 60%
108
(May et al. 2012). So, TP inputs fell from about 20 t y-1 (1.5 g m-2 yr-1) to about 8.5 t
109
y-1 (0.64 g m-2 yr-1). This lower level of TP input was sustained until at least 2005,
110
when a TP load of 8 t y-1 (0.6 g m-2 yr-1) was recorded (May et al. 2012).
111
112
Most of the reduction in TP input was due to better control of effluents from waste
113
water treatment works and industrial sources, between 1987 and 1993 (May et al.
114
2012). However, minor changes aimed at addressing inputs from diffuse sources
115
(such as the installation of buffer strips) were also made (Castle et al. 1999). Key
116
changes in the physics, chemistry and biology of Loch Leven over the pre-
117
management, management and post-management periods have been reported
118
elsewhere (May & Spears, 2012). In summary, these include an increase in growing
119
depth and areal coverage of submerged macrophytes (May & Carvalho 2010; Dudley
120
et al. 2012), a decrease in macroinvertebrate abundance and an increase in the number
121
of taxa (Gunn et al. 2012), improvements in fish populations (Winfield et al. 2012),
122
and an increase in the abundance of aquatic birds that depend on the lake for food and
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May et al – Rotifers in Loch Leven
123
habitat (Carss et al. 2012). Little information on the response of the rotifer community
124
has been published to date.
125
126
Sample collection
127
Water samples were collected at weekly intervals between 1977 and 1982, and
128
fortnightly intervals 1991-1998 and 2010-2011. Sampling methods remained more or
129
less consistent throughout the study period, with plankton and water chemistry
130
samples collected from an open water site with a water depth of about 4 m (“Reed
131
Bower”, Figure 1) using a weighted PVC tube with an internal diameter of 25 mm.
132
Surface samples were also collected close to the outflow (“Sluices”, Figure 1). On
133
some occasions, e.g. during bad weather, these were the only samples collected.
134
135
On return to the laboratory, water samples for chemistry and chlorophyll a analyses
136
were shaken and sub-sampled. Those for TP analysis remained unfiltered; those for
137
chlorophyll a analysis were filtered through a Whatman® GF/C grade filter within 6
138
hours of collection. Filter papers were stored frozen at -18oC prior to analysis.
139
140
Total phosphorus and chlorophyll a analyses
141
Total phosphorus concentrations were determined on samples that were digested with
142
a solution of sulphuric acid and potassium persulphate, following the method
143
described for TP by Wetzel and Likens (2000), with an additional acidification step.
144
This involved adding 0.1 ml of 30% H2SO4 to the samples before adding persulphate.
145
Phosphorus concentrations were determined on a spectrophotometer following the
146
method of Murphy and Riley (1962).
147
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May et al – Rotifers in Loch Leven
148
For chlorophyll a determinations, the frozen filter papers were submerged in 90%
149
methanol overnight in a dark refrigerator. After centrifugation, the extracted
150
chlorophyll a was measured spectrophotometrically at 665 nm with a turbidity
151
correction conducted at 750 nm. Concentrations were determined using equation 1 of
152
APHA (1992).
153
154
Rotifer community analysis
155
Rotifer samples were narcotised in the field by adding sufficient procaine
156
hydrochloride (NH2.C6H4.COO.CH2.CH2.N(C2H5)2.HCl) to give a final concentration
157
of 0.2 g l−1 (May 1985). This ensured that soft bodied species, such as Synchaeta,
158
would be recognisable in the fixed samples. Samples were then preserved in 4%
159
formaldehyde and concentrated by sedimentation. Multiple sub-samples of the
160
concentrate with an individual volume of 3 ml (1977-1982, and 1991-1998) or 5 ml
161
(2010-2011) were counted under ×100 magnification until at least 200 rotifers, or the
162
whole sample, had been counted. Species identifications (following Koste 1978) were
163
carried out on live specimens collected separately from the preserved samples,
164
because many species cannot be fully identified, in preserved samples.
165
3. Results
166
167
168
The 60% reduction in P input to Loch Leven led to a slow but steady decline in
169
annual average open water TP concentrations (Figure 2). Before restoration, these
170
values were about 63 µg P l-1. During and shortly after the P reduction period, the
171
average concentrations rose to about 71 µg P l-1. In the longer term, this value fell to
172
about 34 µg P l-1.
173
7
May et al – Rotifers in Loch Leven
174
Annual mean chlorophyll a (chla) concentrations showed a similar pattern of
175
reduction (Figure 3). Before restoration, these values were about 31 µg chla l-1.
176
During and immediately after management intervention, these values increased to
177
about 47 µg chla l-1. In the longer term, the values fell to about 23 µg chla l-1.
178
179
Similar to P and chlorophyll a concentrations, total annual mean rotifer densities
180
followed a steady decline throughout the restoration period (Figure 4). Before
181
restoration, average annual rotifer population densities were about 1000 ind. l-1.
182
During the P reduction phase and shortly afterwards, these values fell to about
183
630 ind. l-1. Although the rotifer data are less complete than the TP and chlorophyll a
184
data, these lower population densities appeared to be maintained in the longer term,
185
with the equivalent value for 2010-2011 being about 604 ind. l-1. This represented an
186
overall reduction in rotifer numbers of about 40%. However, while both TP and
187
chlorophyll a concentrations initially increased before showing appreciable decreases
188
from 2000 onwards, rotifers densities responded to the change in P load almost
189
immediately. Their numbers had declined by about 40% by the mid 1990s.
190
191
Changes in species diversity over the study period are shown in Table 1. The 13 most
192
common and more abundant species remained in the lake over the entire study period.
193
Although their absolute abundances fell, in line with the overall reduction in total
194
rotifer numbers, their relative abundances remained similar throughout (Figure 5).
195
The most noticeable exceptions to this were the relative proportion of Keratella tecta
196
in relation to the total number of rotifers, and of the ratio of this species to the
197
abundance of Keratella cochlearis. Both of these values decreased over time. The
8
May et al – Rotifers in Loch Leven
198
proportion of Pompholyx sulcata within the rotifer community as a whole also
199
decreased.
200
201
The main changes in species diversity were observed amongst the less common
202
species, which represented only 14%-17% of the rotifer community. Of these,
203
Colurella adriatica and Polyarthra euryptera were lost in the longer term. Collotheca
204
mutabilis, Conochilus hippocrepis, Polyrathra major and Synchaeta oblonga were
205
recorded for the first time during the period of P load reduction and remained in the
206
lake thereafter. Kellicottia longispina, Polyarthra vulgaris and Synchaeta tremula
207
were recorded during the P load reduction period, only, but not in the longer term.
208
209
4. Discussion
210
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When the P input to Loch Leven was reduced by about 60%, the rotifer community
212
responded almost immediately with a reduction of 40% in its annual mean densities.
213
This was in contrast to TP and chlorophyll a concentrations, which showed a lag of
214
several years before beginning to decline. The reduction in rotifer abundance
215
associated with the reduction in TP inputs to Loch Leven is consistent with
216
expectations based on earlier studies of eutrophication impacts. These showed that
217
higher levels of rotifer abundance are associated with increasing levels of
218
eutrophication across a range of different lake types (Blancher 1984, Karabin 1985,
219
Walz et al 1987, Berzins & Pejler 1989; Matveeva 1991; Jeppesen et al. 2000;
220
Duggan et al. 2001; Tasevska et al. 2012) and within individual lakes (Matveeva
221
1986; Walz et al. 1987; Balvay & Laurent 1990; May & O’Hare 2005; Ejsmont-
222
Karabin 1996; Muirhead et al. 1996; Ejsmont-Karabin 2003; Steinberg et al 2009).
223
The results suggest that total rotifer abundance is a good indicator of both
9
May et al – Rotifers in Loch Leven
224
eutrophication and recovery, and that it responds more rapidly to change than other
225
determinands that are used to measure change in water quality more routinely, such as
226
TP and chlorophyll a concentrations.
227
228
At the species level, many authors have reported a strong relationship between certain
229
rotifer ‘indicator’ species and lake trophic state. For example, based on contemporary
230
studies across a number of lakes, it has been reported that more eutrophic
231
environments are more likely to have species such as Brachionus angularis, Filina
232
longiseta, Keratella cochlearis, Keratella tecta, Keratella quadrata, Pompholyx
233
sulcata and Trichocerca pusilla, than less eutrophic environments (Pejler 1983:
234
Karabin 1985; Berzins & Pejler 1989; Matveeva 1991; Ejsmont-Karabin 2003). Many
235
authors have also reported a greater proportion of Keratella tecta in rotifer
236
communities as an indicator of increasing lake trophic state (Hillbricht-Ilkowska
237
1972; Pejler 1981; Karabin 1985; Berzins & Pejler 1989; Ejsmont-Karabin 2012).
238
However, Ejsmont-Karabin & Hillbricht-Ilkowska (1994) suggest that it is unlikely
239
that all of these indicators of trophic state determined across a range of lakes will also
240
reflect in-lake changes in water quality when conditions change. The current study on
241
Loch Leven provides an opportunity for this hypothesis to be explored. In general, the
242
results suggest that the species composition of the rotifer community in Loch Leven,
243
and the proportional contribution of each species to overall abundance, changed very
244
little during the recovery period. However, there was some evidence that the
245
proportion of Keratella tecta increased in relation to overall rotifer abundance as
246
water quality improved, as did the ratio of Keratella tecta:Keratella cochlearis. So,
247
the results of this study support the hypothesis posed by Ejsmont-Karabin &
248
Hillbricht-Ilkowska (1994) that, although overall rotifer abundance is a good,
10
May et al – Rotifers in Loch Leven
249
dynamic indicator of change in the level of trophy of a given lake, other indicators –
250
such as species composition – are less useful. The results also suggest that the
251
proportion of Keratella tecta in relation to total rotifer abundance, and in relation to
252
the abundance of Keratella cochlearis, may be a suitable indicator for monitoring in-
253
lake change in water quality, especially trophic state.
254
255
The results of this study suggest that even simple measures of rotifer abundance and
256
relative species composition could provide sensitive indicators of changing water
257
quality within a lake in response to the control of eutrophication by management
258
intervention. They also suggest that the rotifer community responds to change at a
259
much faster rate than the more commonly used metrics of TP and chlorophyll a
260
concentration, both of which may actually increase during the early stages of
261
recovery. However, such rotifer-based indices must be developed and applied with
262
care, as recent studies have also suggested that the response of zooplankton
263
communities in recovering lakes can be subject to a number of confounding factors,
264
such as changes in fish predation, climate change and other chemical stressors, such
265
as acidification (e.g. Jeppesen et al. 2005), that make results difficult to interpret. This
266
is especially true where water quality in general, and rotifer populations in particular,
267
are influenced by multiple stressors.
268
269
5. Acknowledgements
270
271
We thank the Montgomery family, who own Loch Leven, for their help with and
272
support for this work over the last 44 years. This research was funded by the Natural
273
Environment Research Council, UK, with some small contributions from Scottish
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May et al – Rotifers in Loch Leven
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Natural Heritage and the Scottish Environment Protection Agency. Loch Leven is part
275
of the UK Environmental Change Network (http://www.ecn.ac.uk/).
276
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7. Tables
444
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Table 1. Rotifer species found in Loch Leven over different time periods
Species
1977-1982
1991-1998
2010-2011
Asplanchna priodonta Gosse
X
X
X
Brachionus angularis Gosse
X
X
X
Conochilus unicornis Rousselet
X
X
X
Filinia longiseta (Ehrenberg)
X
X
X
Keratella cochlearis (Gosse)
X
X
X
Keratella quadrata (Müller)
X
X
X
Keratella tecta (Gosse)
X
X
X
Notholca squamula (Müller)
X
X
X
Polyarthra dolichoptera Idelson
X
X
X
Pompholyx sulcata Hudson
X
X
X
Synchaeta grandis Zacharias
X
X
X
Synchaeta kitina Rousselet
X
X
X
Trichocerca pusilla (Jennings)
X
X
X
Colurella adriatica Ehrenberg
X
X
-
Polyarthra euryptera Wierzejski
X
X
-
Conochilus hippocrepis (Schrank)
-
X
X
Collotheca mutabilis Hudson
-
X
X
Polyarthra major Burckhardt
-
X
X
Synchaeta oblonga Ehrenberg
-
X
X
Kellicottia longispina (Kellicott)
-
X
-
Polyarthra vulgaris Carlin
-
X
-
Synchaeta tremula (Müller)
-
X
-
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May et al – Rotifers in Loch Leven
8. Figure legends
447
448
449
Figure 1. Map of Loch Leven, showing routine sampling sites (squares), inflows and
450
outflow (River Leven) (____), major roads (
451
Ordnance Survey Strategi dataset. Contains Ordnance Survey data © Crown copyright
452
and database right 2012.
___
) and urban areas (grey). Map data from
453
454
Figure 2. Annual mean total phosphorus (TP) concentrations in Loch Leven, 1977-
455
2011.
456
457
Figure 3. Annual mean chlorophyll a concentrations in Loch Leven, 1977-2011.
458
459
Figure 4. Annual mean total rotifer densities in Loch Leven, 1977-1982, 1992-1998
460
and 2010-2011.
461
462
Figure 5. Relative abundances of common and less common (‘other’) rotifer species
463
in Loch Leven, 1977-1982, 1992-1998 and 2010-2011.
464
19
Figure 1.
µg L-1
100
90
80
70
60
50
40
30
20
10
0
1970
Figure 2
Annual mean TP concentration
1980
1990
2000
2010
2020
Figure 3
Annual mean rotifer density
ind. L-1
1600
1200
800
400
0
1970
Figure 4
1980
1990
2000
2010
2020
1991-1998
1977-1982
2010-2011
Keratella tecta
Keratella cochlearis
Synchaeta kitina
Trichocerca pusilla
Pompholyx sulcata
Polyarthra dolichoptera
Other species
Figure 5